Ocean warming and acidification alter the behavioral response to flow of the sea urchin Paracentrotus lividus

Abstract

Ocean warming (OW) and acidification (OA) are intensively investigated as they pose major threats to marine organism. However, little effort is dedicated to another collateral climate change stressor, the increased frequency, and intensity of storm events, here referred to as intensified hydrodynamics. A 2‐month experiment was performed to identify how OW and OA (temperature: 21°C; pHT: 7.7, 7.4; control: 17°C‐pHT7.9) affect the resistance to hydrodynamics in the sea urchin Paracentrotus lividus using an integrative approach that includes physiology, biomechanics, and behavior. Biomechanics was studied under both no‐flow condition at the tube foot (TF) scale and flow condition at the individual scale. For the former, TF disk adhesive properties (attachment strength, tenacity) and TF stem mechanical properties (breaking force, extensibility, tensile strength, stiffness, toughness) were evaluated. For the latter, resistance to flow was addressed as the flow velocity at which individuals detached. Under near‐ and far‐future OW and OA, individuals fully balanced their acid‐base status, but skeletal growth was halved. TF adhesive properties were not affected by treatments. Compared to the control, mechanical properties were in general improved under pHT7.7 while in the extreme treatment (21°C‐pHT7.4) breaking force was diminished. Three behavioral strategies were implemented by sea urchins and acted together to cope with flow: improving TF attachment, streamlining, and escaping. Behavioral responses varied according to treatment and flow velocity. For instance, individuals at 21°C‐pHT7.4 increased the density of attached TF at slow flows or controlled TF detachment at fast flows to compensate for weakened TF mechanical properties. They also showed an absence of streamlining favoring an escaping behavior as they ventured in a riskier faster movement at slow flows. At faster flows, the effects of OW and OA were detrimental causing earlier dislodgment. These plastic behaviors reflect a potential scope for acclimation in the field, where this species already experiences diel temperature and pH fluctuations.

Do males and females respond differently to ocean acidification? An experimental study with the sea urchin Paracentrotus lividus

“…Although in our study pH significantly influenced respiration rate after 21 days, no significant effects of pH were observed after 40 days of exposure. This suggested that both male and female P. lividus have the potential to acclimate at low pH conditions after prolonged exposure, as already observed for the same species, both in a laboratory 2-months exposure (Cohen-Rengifo et al 2019) and in specimens from CO 2 vents at Ischia Island (Migliaccio et al 2019). Similarly, in other species, namely E. mathaei, Strongylocentrotus fragilis, Strongylocentrotus droebachiensis, and Echinometra sp.…”

“…Only extremely low pH (6.6) negatively affected righting time in S. fragilis (Taylor et al 2014 ). Other behavioural aspects in P.lividus were recently investigated by Cohen-Rengifo et al ( 2019 ). They showed that podia adhesion strength was not influenced by reduced pH and highlighted positive synergistic effects of ocean acidification and ocean warming on sea urchin moving velocity at 7.7 pH, but not at 7.4 pH.…”

“…It was hypothesized that the observed behavioural modifications were ascribed to the accumulation of HCO 3 − in extracellular fluid, as protection against acidosis, and to the compensatory reduction of Cl − (Stumpp et al 2012 ; Collard et al 2014 ). Alterations in the concentration of these ions could influence GABA receptors, which are involved in neurological mechanisms, such as information processing (Cohen-Rengifo et al 2019 ). Potential modifications of sea urchin behaviour under reduced pH deserve further attention in future studies.…”

“…However, in this species, coelomic fluid pH seems to be only partially compensated at extreme pH condition (7.4 pH). This compensation of the coelomic fluid pH in P. lividus was not dependent on skeleton dissolution, indeed skeletal mechanical properties were not affected at 7.7 pH (Catarino et al 2012 ; Collard et al 2013 , 2014 , 2016 ; Cohen-Rengifo et al 2019 ). The acid-base regulation capability allows sea urchins to maintain appropriate extracellular and intracellular pH conditions, but the processes involved in this regulation are energy-consuming and lead to increased oxygen uptake.…”

Combined effect of microplastics and global warming factors on early growth and development of the sea urchin (Paracentrotus lividus)

“…For instance, larvae of the sea urchin Arbacia lixula grown at low pH exhibited reduced arm length (Foo et al, 2020). Although it was demonstrated that under near-and far-future ocean warming and acidification scenarios individuals of Paracentrotus lividus fully balanced their acid-base status, their skeletal growth was halved after 60 days (Rengifo et al, 2019). Thus, it is evident that the study of the effects of multi-stressor scenarios is crucial to have a realistic scheme of the impact that human activities are causing to aquatic life.…”